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Drug Evaluation

Fruquintinib as new treatment option in metastatic colorectal cancer patients: is there an optimal sequence?

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Pages 371-382 | Received 23 Jan 2024, Accepted 25 Mar 2024, Published online: 03 Apr 2024

References

  • Argilés G, Tabernero J, Labianca R, et al. Localised colon cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up†. Ann Oncol. 2020;31(10):1291–1305. doi: 10.1016/j.annonc.2020.06.022
  • Mrozovski JM. Cancer colorectal. Actual Pharm. 2023;62(623):49–51. doi: 10.1016/j.actpha.2023.01.013
  • Cervantes A, Adam R, Roselló S, et al. Metastatic colorectal cancer: ESMO clinical practice guideline for diagnosis, treatment and follow-up ☆. Ann Oncol. 2023;34(1):10–32. doi: 10.1016/j.annonc.2022.10.003
  • Van Cutsem E, Lenz H-J, Köhne C-H, et al. Fluorouracil, leucovorin, and irinotecan plus cetuximab treatment and RAS mutations in colorectal cancer. J Clin Oncol. 2015;33(7):692–700. doi: 10.1200/JCO.2014.59.4812
  • Douillard J-Y, Oliner KS, Siena S, et al. Panitumumab–FOLFOX4 treatment and RAS mutations in colorectal cancer. N Engl J Med. 2013;369(11):1023–1034. doi: 10.1056/nejmoa1305275
  • Venook AP, Niedzwiecki D, Innocenti F et al. Impact of primary (1º) tumor location on overall survival (OS) and progression-free survival (PFS) in patients (pts) with metastatic colorectal cancer (mCRC): analysis of CALGB/SWOG 80405 (alliance). J Clin Oncol. 2016 May;34(15_suppl):3504–3504.
  • Lavacchi D, Roviello G, Guidolin A, et al. Evaluation of fruquintinib in the continuum of care of patients with colorectal cancer. Int J Mol Sci. 2023;24(6):5840. doi: 10.3390/ijms24065840
  • Abrams TA, Meyer G, Schrag D, et al. Chemotherapy usage patterns in a US-wide cohort of patients with metastatic colorectal cancer. J Natl Cancer Inst. 2014;106(2):1–10. doi: 10.1093/jnci/djt371
  • Boyne DJ, Ngan E, Carbonell C, et al. Real-world study to assess patterns of treatment practices and clinical outcomes in metastatic colorectal cancer patients with RAS wild-type left-sided tumours in Canada. Curr Oncol. 2023;30(9):8220–8232. doi: 10.3390/curroncol30090596
  • Rossini D, Germani MM, Lonardi S, et al. Treatments after second progression in metastatic colorectal cancer: a pooled analysis of the TRIBE and TRIBE2 studies. Eur J Cancer. 2022 Jul;170:64–72. doi: 10.1016/j.ejca.2022.04.019
  • Aranda E, Polo E, Camps C, et al. Treatment patterns for metastatic colorectal cancer in Spain. Clin Transl Oncol. 2020;22(9):1455–1462. doi: 10.1007/s12094-019-02279-5
  • Dasari A, Lonardi S, Garcia-Carbonero R, et al. Fruquintinib versus placebo in patients with refractory metastatic colorectal cancer (FRESCO-2): an international, multicentre, randomised, double-blind, phase 3 study. Lancet. 2023;402(10395):41–53. doi: 10.1016/S0140-6736(23)00772-9
  • Dasari A, Sobrero A, Yao J, et al. FRESCO-2: a global phase III study investigating the efficacy and safety of fruquintinib in metastatic colorectal cancer. Futur Oncol. 2021;17(24):3151–3162. doi: 10.2217/fon-2021-0202
  • Mabeta P, Steenkamp V. The VEGF/VEGFR axis revisited: implications for cancer therapy. Int J Mol Sci. 2022;23(24). doi: 10.3390/ijms232415585
  • Geindreau M, Ghiringhelli F, Bruchard M. Vascular endothelial growth factor, a key modulator of the anti-tumor immune response. Int J Mol Sci. 2021;22(9). doi: 10.3390/ijms22094871
  • Lacal PM, Graziani GTherapeutic implication of vascular endothelial growth factor receptor-1 (VEGFR-1) targeting in cancer cells and tumor microenvironment by competitive and non-competitive inhibitors. Pharmacol Res. 2018 Oct;136:97–107. doi: 10.1016/j.phrs.2018.08.023
  • Melincovici CS, Boşca, AB, Şuşman S et al. Vascular endothelial growth factor (VEGF) - key factor in normal and pathological angiogenesis. Rom J Morphol Embryol = Rev Roum Morphol Embryol. 2018;59(2):455–467.
  • Rahimi N. VEGFR-1 and VEGFR-2: two non-identical twins with a unique physiognomy. Front Biosci. 2006;11(1):447–888, pp. 818–829. doi:10.2741/1839
  • Zhong M, Li N, Qiu X, et al. TIPE regulates VEGFR2 expression and promotes angiogenesis in colorectal cancer. Int J Biol Sci. 2020;16(2):272–283. doi: 10.7150/ijbs.37906
  • Rapisarda A, Melillo G. Role of the VEGF/VEGFR axis in cancer biology and therapy. Adv Cancer Res. 2012;114:237–267. doi: 10.1016/B978-0-12-386503-8.00006-5
  • Coso S, Zeng Y, Opeskin K, et al. Vascular endothelial growth factor receptor-3 directly interacts with phosphatidylinositol 3-kinase to regulate lymphangiogenesis. PloS One. 2012;7(6):e39558. doi: 10.1371/journal.pone.0039558
  • Su J-L, Yen C-J, Chen P-S, et al. The role of the VEGF-C/VEGFR-3 axis in cancer progression. Br J Cancer. 2007 Feb;96(4):541–545.
  • Zhang Y, Zou JY, Wang Z, et al. Fruquintinib: a novel antivascular endothelial growth factor receptor tyrosine kinase inhibitor for the treatment of metastatic colorectal cancer. Cancer Manag Res. 2019;11:7787–7803. doi: 10.2147/CMAR.S215533
  • Li AY, McCusker MG, Russo A, et al. RET fusions in solid tumors. Cancer Treat Rev. 2019 Dec;81:101911. doi: 10.1016/j.ctrv.2019.101911
  • Katoh M. FGFR inhibitors: effects on cancer cells, tumor microenvironment and whole-body homeostasis (review). Int J Mol Med. 2016 Jul;38(1):3–15. doi: 10.3892/ijmm.2016.2620
  • Stankov K, Popovic S, Mikov M. C-KIT signaling in cancer treatment. Curr Pharm Des. 2014;20(17):2849–2880. doi: 10.2174/13816128113199990593
  • Troiani T, Martinelli E, Orditura M, et al. Beyond bevacizumab: new anti-VEGF strategies in colorectal cancer. Expert Opin Investig Drugs. 2012;21(7):949–959. doi: 10.1517/13543784.2012.689287
  • Shibuya M. Vascular endothelial growth factor (VEGF) and its receptor (VEGFR) signaling in angiogenesis: a crucial target for anti- and pro-angiogenic therapies. Genes Cancer. 2011;2(12):1097–1105. doi: 10.1177/1947601911423031
  • Grothey A, Sugrue MM, Purdie DM, et al. Bevacizumab beyond first progression is associated with prolonged overall survival in metastatic colorectal cancer: results from a large observational cohort study (BRiTE). J Clin Oncol. 2008;26(33):5326–5334. doi: 10.1200/JCO.2008.16.3212
  • Hurwitz HI, Bekaii-Saab, TS, Bendell, JC et al. Safety and effectiveness of bevacizumab treatment for metastatic colorectal cancer: final results from the Avastin® registry - investigation of effectiveness and safety (ARIES) observational cohort study. Clin Oncol. 2014;26(6):323–332. doi: 10.1016/j.clon.2014.03.001
  • Klement G, Baruchel S, Rak J, et al. Continuous low-dose therapy with vinblastine and VEGF receptor-2 antibody induces sustained tumor regression without overt toxicity. J Clin Invest. 2000;105(8):R15–R24. doi: 10.1172/JCI8829
  • Melnyk O, Zimmerman M, Kim KJIN, et al. Neutralizing anti-vascular endothelial growth factor antibody inhibits further growth of established prostate cancer and metastases in a pre-clinical model. J Urol. 1999;161(3):960–963. doi: 10.1016/s0022-5347(01)61829-9
  • Bennouna J, Sastre J, Arnold D, et al. Continuation of bevacizumab after first progression in metastatic colorectal cancer (ML18147): a randomised phase 3 trial. Lancet Oncol. 2013;14(1):29–37. doi: 10.1016/S1470-2045(12)70477-1
  • Masi G, Salvatore L, Boni L, et al. Continuation or reintroduction of bevacizumab beyond progression to first-line therapy in metastatic colorectal cancer: final results of the randomized BEBYP trial. Ann Oncol. 2015;26(4):724–730. doi: 10.1093/annonc/mdv012
  • Bennouna J, Hiret S, Borg C et al. Bevacizumab (Bev) or cetuximab (Cet) plus chemotherapy after progression with bevacizumab plus chemotherapy in patients with wild-type (WT) KRAS metastatic colorectal cancer (mCRC): final analysis of a French randomized, multicenter, phase II study (PRODIGE 18). Ann Oncol. 2017;28:v159–v160. doi: 10.1093/annonc/mdx393.004
  • Hecht JR, Cohn A, Dakhil S, et al. SPIRITT: a randomized, multicenter, phase II study of Panitumumab with FOLFIRI and Bevacizumab with FOLFIRI as second-line treatment in patients with unresectable wild type KRAS metastatic colorectal cancer. Clin Colorectal Cancer. 2015;14(2):72–80. doi: 10.1016/j.clcc.2014.12.009
  • Van Cutsem E, Tabernero J, Lakomy R, et al. Addition of aflibercept to fluorouracil, leucovorin, and irinotecan improves survival in a phase III randomized trial in patients with metastatic colorectal cancer Previously treated with an oxaliplatin-based regimen. J Clin Oncol. 2012;30(28):3499–3506. doi: 10.1200/JCO.2012.42.8201
  • Tabernero J, Yoshino T, Cohn AL, et al. Ramucirumab versus placebo in combination with second-line FOLFIRI in patients with metastatic colorectal carcinoma that progressed during or after first-line therapy with bevacizumab, oxaliplatin, and a fluoropyrimidine (RAISE): a randomised, double-blin. Lancet Oncol. 2015;16(5):499–508. doi: 10.1016/S1470-2045(15)70127-0
  • Grothey A, Cutsem EV, Sobrero A, et al. Regorafenib monotherapy for previously treated metastatic colorectal cancer (CORRECT): an international, multicentre, randomised, placebo-controlled, phase 3 trial. Lancet (London, England). 2013 Jan;381(9863):303–312.
  • Prager GW, Taieb J, Fakih M et al. Trifluridine-tipiracil and Bevacizumab in refractory metastatic colorectal cancer. N Engl J Med. 2023 May;388(18):1657–1667. doi: 10.1056/NEJMoa2214963
  • Sun Q, Zhou J, Zhang Z, et al. Discovery of fruquintinib, a potent and highly selective small molecule inhibitor of VEGFR 1, 2, 3 tyrosine kinases for cancer therapy. Cancer Biol Ther. 2014;15(12):1635–1645. doi: 10.4161/15384047.2014.964087
  • Gu Y, Wang J, Li K, et al. Preclinical pharmacokinetics and disposition of a novel selective VEGFR inhibitor fruquintinib (HMPL-013) and the prediction of its human pharmacokinetics. Cancer Chemother Pharmacol. 2014 Jul;74(1):95–115.
  • Fakih M, Raghav KPS, Chang DZ, et al. Regorafenib plus nivolumab in patients with mismatch repair-proficient/microsatellite stable metastatic colorectal cancer: a single-arm, open-label, multicentre phase 2 study. EClinicalMedicine. 2023 Apr;58:101917. doi: 10.1016/j.eclinm.2023.101917
  • Li Q, Cheng X, Zhou C, et al. Fruquintinib enhances the antitumor immune responses of anti-programmed death receptor-1 in colorectal cancer. Front Oncol. 2022;12:841977. doi: 10.3389/fonc.2022.841977
  • Li J, Qin S, Xu R-H, et al. Effect of fruquintinib vs placebo on overall survival in patients with previously treated metastatic colorectal cancer: the FRESCO randomized clinical trial. JAMA. 2018 Jun;319(24):2486–2496. doi: 10.1001/jama.2018.7855
  • Shirley M. Fruquintinib: first global approval. Drugs. 2018 Nov;78(16):1757–1761. doi: 10.1007/s40265-018-0998-z
  • Zhang Q, Wang Q, Wang X, et al. Regorafenib, TAS-102, or fruquintinib for metastatic colorectal cancer: any difference in randomized trials? Int J Colorectal Dis. 2020 Feb;35(2):295–306. doi: 10.1007/s00384-019-03477-x
  • Li J, Qin S, Xu R, et al. Regorafenib plus best supportive care versus placebo plus best supportive care in Asian patients with previously treated metastatic colorectal cancer (CONCUR): a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet Oncol. 2015 Jun;16(6):619–629.
  • Mayer RJ, Van Cutsem E, Falcone A, et al. Randomized trial of TAS-102 for refractory metastatic colorectal cancer. N Engl J Med. 2015 May;372(20):1909–1919.
  • Xu J, Kim TW, Shen L, et al. Results of a randomized, double-blind, placebo-controlled, phase III trial of Trifluridine/Tipiracil (TAS-102) monotherapy in Asian patients with Previously treated metastatic colorectal cancer: the TERRA study. J Clin Oncol Off J Am Soc Clin Oncol. 2018 Feb;36(4):350–358.
  • Moriwaki T, Fukuoka S, Taniguchi H, et al. Propensity Score analysis of regorafenib versus trifluridine/tipiracil in patients with metastatic colorectal cancer refractory to standard chemotherapy (REGOTAS): a Japanese society for cancer of the colon and rectum multicenter observational study. Oncology. 2018 Jan;23(1):7–15.
  • Nevala-Plagemann C, Sama S, Ying J, et al. A real-world comparison of regorafenib and trifluridine/tipiracil in refractory metastatic colorectal cancer in the United States. J Natl Compr Canc Netw. 2023 Feb;21(3):257–264.
  • Sueda T, Sakai D, Kudo T, et al. Efficacy and safety of regorafenib or TAS-102 in patients with metastatic colorectal cancer refractory to standard therapies. Anticancer Res. 2016 Aug;36(8):4299–4306.
  • Masuishi T,Taniguchi H, Hamauchi S, et al. Regorafenib versus trifluridine/tipiracil for refractory metastatic colorectal cancer: a retrospective comparison. Clin Colorectal Cancer. 2017 Jun;16(2):e15–e22.
  • Dasari A, Lonardi S, Garcia-Carbonero R, et al. Subgroup analyses of safety and efficacy by number and types of prior lines of treatment in FRESCO-2, a global phase III study of fruquintinib in patients with refractory metastatic colorectal cancer. J Clin Oncol. 2023 May;41(16_suppl):3604.
  • Garcia-Carbonero R, Van Cutsem E, Ciardiello F et al. Subgroup analysis of patients with metastatic colorectal cancer (mCRC) treated with regorafenib (REG) in the phase 3b CONSIGN trial who had progression-free survival (PFS) >4 months (m). Ann Oncol. 2016;27(Supplement 6):vi167. doi: 10.1093/annonc/mdw370.54
  • Fukuoka S, Moriwaki T, Taniguchi H, et al. Regorafenib (REG) versus trifluridine/tipiracil (TAS-102) as salvage-line in patients with metastatic colorectal cancer refractory to standard chemotherapies (REGOTAS): a propensity score analysis from a JSCCR multicenter observational study. J Clin Oncol. 2017 May;35(15_suppl):3540.
  • Schulz H, Janssen J, Strauss UP, et al. Clinical efficacy and safety of regorafenib (REG) in the treatment of metastatic colorectal cancer (mCRC) in daily practice in Germany: final results of the prospective multicentre non-interventional RECORA study. J Clin Oncol. 2018 Feb;36(4_suppl):748.
  • Adenis A, de la Fouchardiere C, Paule B, et al. Erratum to: survival, safety, and prognostic factors for outcome with regorafenib in patients with metastatic colorectal cancer refractory to standard therapies: results from a multicenter study (REBECCA) nested within a compassionate use program. BMC Cancer. 2016 Jul;16(1):518.
  • Grothey A, Huang L, Wagner A, et al. Hand-foot skin reaction (HFSR) and outcomes in the phase 3 CORRECT trial of regorafenib for metastatic colorectal cancer (mCRC). J Clin Oncol. 2017 May;35(15_suppl):3551. doi: 10.1200/JCO.2017.35.15_suppl.3551
  • Li J,Qin S, Bai Y et al. Association between hand-foot skin reaction (HFSR) and survival benefit of fruquintinib in FRESCO trial. J Clin Oncol. 2019;37(15_suppl):e15012–15012. doi: 10.1200/jco.2019.37.15_suppl.e15012
  • Antoniotti C, Marmorino F, Boccaccino A, et al. Early modulation of angiopoietin-2 plasma levels predicts benefit from regorafenib in patients with metastatic colorectal cancer. Eur J Cancer. 2022 Apr;165:116–124. doi: 10.1016/j.ejca.2022.01.025
  • Cosso F, Lavacchi D, Fancelli S, et al. Long-term response of more than 9 years to regorafenib in a heavily pretreated patient with metastatic colorectal cancer. Anticancer Drugs. 2023 Mar;34(3):451–454.
  • Marmorino F, Salvatore L, Barbara C, et al. Serum LDH predicts benefit from bevacizumab beyond progression in metastatic colorectal cancer. Br J Cancer. 2017 Jan;116(3):318–323.
  • Iorio J, Lastraioli E, Tofani L, et al. hERG1 and HIF-2α behave as biomarkers of positive response to Bevacizumab in metastatic colorectal cancer patients. Transl Oncol. 2020 Mar;13(3):100740.
  • van de Haar J, Ma X, Ooft SN, et al. Codon-specific KRAS mutations predict survival benefit of trifluridine/tipiracil in metastatic colorectal cancer. Nat Med. 2023 Mar;29(3):605–614.
  • Strickler JH, Cercek A, Siena S, et al. Tucatinib plus trastuzumab for chemotherapy-refractory, HER2-positive, RAS wild-type unresectable or metastatic colorectal cancer (MOUNTAINEER): a multicentre, open-label, phase 2 study. Lancet Oncol. 2023 May;24(5):496–508.
  • Yoshino T, Di Bartolomeo M, Raghav K, et al. Final results of DESTINY-CRC01 investigating trastuzumab deruxtecan in patients with HER2-expressing metastatic colorectal cancer. Nat Commun. 2023 Jun;14(1):3332.
  • Cremolini C, Montagut C, Ronga P, et al. Rechallenge with anti-EGFR therapy to extend the continuum of care in patients with metastatic colorectal cancer. Front Oncol. 2022;12:946850. doi: 10.3389/fonc.2022.946850
  • Henry JT. Comprehensive clinical and molecular characterization of KRAS G12C -mutant colorectal cancer. JCO Precis Oncol. 2021;5(5):613–621.
  • Siena S, Sartore-Bianchi A, Marsoni S, et al. Targeting the human epidermal growth factor receptor 2 (HER2) oncogene in colorectal cancer. Ann Oncol Off J Eur Soc Med Oncol. 2018 May;29(5):1108–1119.
  • Tabernero J,Grothey A, Van Cutsem E et al. Encorafenib plus Cetuximab as a new standard of care for Previously treated BRAF V600E-Mutant metastatic colorectal cancer: updated survival results and subgroup analyses from the BEACON study. J Clin Oncol Off J Am Soc Clin Oncol. 2021 Feb;39(4):273–284.
  • Fakih MG, Salvatore L, Esaki T, et al. Sotorasib plus Panitumumab in refractory colorectal cancer with mutated KRAS G12C. N Engl J Med. 2023 Dec;389(23):2125–2139.
  • Lonardi S, Pietrantonio F. New options for late-line treatment of metastatic colorectal cancer. Nat Rev Gastroenterol Hepatol. 2023 Dec;21(2):76–77. doi: 10.1038/s41575-023-00881-1
  • Sartore-Bianchi A, Pietrantonio F, Lonardi S, et al. Circulating tumor DNA to guide rechallenge with panitumumab in metastatic colorectal cancer: the phase 2 CHRONOS trial. Nat Med. 2022 Aug;28(8):1612–1618.
  • Antoniotti C, Rossini D, Pietrantonio F, et al. Upfront FOLFOXIRI plus bevacizumab with or without atezolizumab in the treatment of patients with metastatic colorectal cancer (AtezoTRIBE): a multicentre, open-label, randomised, controlled, phase 2 trial. Lancet Oncol. 2022 Jul;23(7):876–887.
  • Fukuoka S, Hara H, Takahashi N, et al. Regorafenib plus nivolumab in patients with advanced gastric or colorectal cancer: an open-label, dose-escalation, and dose-expansion phase ib trial (REGONIVO, EPOC1603). J Clin Oncol Off J Am Soc Clin Oncol. 2020 Jun;38(18):2053–2061.
  • Zhang W, Zhang Z, Lou S, et al. Efficacy, safety and predictors of combined fruquintinib with programmed death-1 inhibitors for advanced microsatellite-stable colorectal cancer: a retrospective study. Front Oncol. 2022;12:929342. doi: 10.3389/fonc.2022.929342
  • Zeng J, Baik C, Bhatia S, et al. Combination of stereotactic ablative body radiation with targeted therapies. Lancet Oncol. 2014 Sep;15(10):426–434.
  • Wang K, Chen Y, Zhang Z et al. RIFLE: a phase II trial of stereotactic ablative radiotherapy combined with fruquintinib and tislelizumab in metastatic colorectal cancer. Gastroenterol Rep. 2023;11. doi: 10.1093/gastro/goad063